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Soil legacy and fungal community responses to Cytisus scoparius invasion A thesis submitted in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Biology 2020 Ralph Wainer The University of Canterbury General abstract The goal of my thesis was to study the effects of soil under various levels of invasive Cytisus scoparius (Scotch broom) and then examine whether the unique soil legacy of C. scoparius was contingent on how C. scoparius shaped soil fungal communities. I began my research by studying the effect of the soil legacy of C. scoparius in a controlled environment (via a greenhouse experiment; Chapter 2). Knowing the effect of the soil legacy of C. scoparius under regulated conditions, I then undertook a field survey (via a natural experiment; Chapter 3), in which I systematically recorded changes in fungal community composition across a natural density gradient of C. scoparius invasion. I subsequently investigated whether the environmental DNA (eDNA) metabarcoding techniques I applied throughout my natural survey could be optimised for future researchers (via a methodological experiment; Chapter 4). Lastly, I analysed how different fungal communities found near C. scoparius may underlie the results of my greenhouse experiment (via mixed-effect modelling; Chapter 5). In Chapter 2, I found contrary to my hypothesis that the effects of soil extracted under various levels of C. scoparius invasion favoured the growth of native New Zealand plants over its own taxonomic family in a controlled greenhouse environment. Given that the predominantly positive soil legacy of C. scoparius could only be partly attributed to soil chemical traits, microbial effects likely played an underlying role in the invasion success of C. scoparius. In Chapter 3, I found that fungal diversity in soil under C. scoparius was unexpectedly higher than in grassland uninvaded by C. scoparius, and that C. scoparius invasion resulted in increased homogenisation of certain fungal groups within the overall soil fungal community. My results suggested that coalescence between previously separated fungal communities may have occurred due to C. scoparius invasion. Apart from C. scoparius having a definite effect on soil fungal communities, it is possible that the soil fungal communities themselves might contribute to the shrub’s invasiveness, which I further tested in a field-experiment (Appendix E). In Chapter 4, I present the pitfalls and benefits of eDNA pooling, identifying a fungal taxon-wide bias in the proportional abundance of fungi in pooled eDNA samples. I demonstrate how rarer fungi remain increasingly unaccounted for with increased degrees of pooling, yet also show how pooling may benefit researchers who wish to study the larger-scale effect of environmental drivers (e.g., anthropogenic effects, invasive species impacts). In Chapter 5, I show how increased arbuscular mycorrhizal richness found in more homogenised soil communities (studied in Chapter 1) were partly responsible for the generally positive soil legacy of C. scoparius, especially for exotic Fabaceae which can probably benefit more from arbuscular mycorrhizal fungi-facilitated P enrichment due to their ability to fix N. 1 By demonstrating how changes in fungal communities caused by an invasive N-fixing plant may impact plant growth and nutrient acquisition, the results of my thesis highlight the importance of incorporating fungal community composition in soil legacy studies. Although biodiversity losses of plants and other organisms following invasion are common, I show how soil fungal communities may be considered an exception to the rule. I highlight the importance of systematic sample processing and encourage the use of eDNA metabarcoding techniques to better understand how changes in soil fungal communities may possibly benefit native plants in ecological restoration projects or adversely underlie an exotic shrub’s invasiveness. 2 Deputy Vice-Chancellor’s Office Postgraduate Research Office Co-Authorship Form This form is to accompany the submission of any thesis that contains research reported in co-authored work that has been published, accepted for publication, or submitted for publication. A copy of this form should be included for each co-authored work that is included in the thesis. Completed forms should be included at the front (after the thesis abstract) of each copy of the thesis submitted for examination and library deposit. Please indicate the chapter/section/pages of this thesis that are extracted from co-authored work and provide details of the publication or submission from the extract comes: Community-level direct and indirect impacts of an invasive plant favour exotic over native species – Appendix E Please detail the nature and extent (%) of contribution by the candidate: 50% - The candidate is joint-first author on the published Journal of Ecology research article “Community‐level direct and indirect impacts of an invasive plant favour exotic over native species”, which is included in the Appendix of the thesis. Certification by Co-authors: If there is more than one co-author then a single co-author can sign on behalf of all The undersigned certifies that: ▪ The above statement correctly reflects the nature and extent of the Doctoral candidate’s contribution to this co-authored work ▪ In cases where the candidate was the lead author of the co-authored work he or she wrote the text Name: Warwick Allen Signature: Date: 29/06/2020 3 Acknowledgments This research was funded by the Bio-Protection Research Centre (BPRC) and the National Science Challenge, with additional support from the Ross Beever Memorial Mycological Award. I thank the landowners and the Department of Conservation (DOC) for access to the study sites, Xiao Xiao Lin and the team at Massey Genome Service for their support with sequencing, and Ngaire Foster along with the team at Manaaki Whenua for their help with plant nutrient analysis. The research plots at Molesworth Station were initially established by Manaaki Whenua researchers, including D. Peltzer, M. St John, C. Morse and K. Orwin. I am greatly indebted to my supervisory team, who allowed me to embark on this academic adventure in this beautiful part of the world: Ian, Eirian and Hayley - thank you for all your guidance and support during these last three years and for enabling me to learn many rare lessons. I wouldn’t wish for any other group of supervisors. I am likewise grateful that I could both know and work alongside Warwick Allen and all members of the Ecosystem Mycology Group. My thanks goes to all my collaborators and colleagues at the BPRC, to Lauren, Andi, Sam, Rowan, Jacopo, Andrei, Romy, Tom, Isabelle, Francesco, Aimee, Kuchar, Phil and Will. I am thankful for Angela Wakelin’s, Brigitta Kurenbach’s and Steven Gieseg’s help in the wet-lab, Dave Conder’s cheerful assistance within the greenhouses and for the purchasing powers of both Brian Kwan and Angela Langrish. Alan Woods, Linda Morris, Jennifer Bufford and Andrew Holyoake all helped address unexpected pickles and my fieldwork and sample processing wouldn’t have been possible without the continued aid of many students, especially Georgia, Nils, Laura and Marcus-Rongowhitiao. I am glad to have been able to work alongside Joanna, Vanita, John, Tyler, Sarah, Jonathan and Zach and to have learnt so much from so many. A special shout-out goes to my academic ‘grandparents’, to Rus, Yves, Lilia, Nancy, Mia and Jerzy. My final thanks goes to my parents, to Anna, Christina and Robert for their unending support. 4 Table of Contents General abstract ............................................................................................................................................. 1 Acknowledgments ......................................................................................................................................... 4 Chapter 1: General introduction .................................................................................................................. 6 Chapter 2: The soil legacy of Cytisus scoparius ............................................................................................ 12 Introduction .................................................................................................................................................... 13 Methods ........................................................................................................................................................... 17 Results ............................................................................................................................................................. 23 Discussion ....................................................................................................................................................... 30 Chapter 3: The response of fungal communities to Cytisus scoparius invasion ......................................... 35 Introduction .................................................................................................................................................... 36 Methods ........................................................................................................................................................... 41 Results ............................................................................................................................................................. 46 Discussion ......................................................................................................................................................
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